{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T14:32:11Z","timestamp":1790173931722,"version":"4.1.0"},"reference-count":51,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2019,8,10]],"date-time":"2019-08-10T00:00:00Z","timestamp":1565395200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Escherichia coli may innocuously colonize the intestine of healthy subjects or may instigate infections in the gut or in other districts. This study investigated intestinal E. coli isolated from 20 healthy adults. Fifty-one strains were genotyped by molecular fingerprinting and analyzed for genetic and phenotypic traits, encompassing the profile of antibiotic resistance, biofilm production, the presence of surface structures (such as curli and cellulose), and their performance as recipients in conjugation experiments. A phylogroup classification and analysis of 34 virulence determinants, together with genes associated to the pks island (polyketide-peptide genotoxin colibactin) and conjugative elements, was performed. Most of the strains belonged to the phylogroups B1 and B2. The different phylogroups were separated in a principal coordinate space, considering both genetic and functional features, but not considering pulsed-field gel electrophoresis. Within the B2 and F strains, 12 shared the pattern of virulence genes with potential uropathogens. Forty-nine strains were sensitive to all the tested antibiotics. Strains similar to the potential pathogens innocuously inhabited the gut of healthy subjects. However, they may potentially act as etiologic agents of extra-intestinal infections and are susceptible to a wide range of antibiotics. Nevertheless, there is still the possibility to control infections with antibiotic therapy.<\/jats:p>","DOI":"10.3390\/microorganisms7080251","type":"journal-article","created":{"date-parts":[[2019,8,12]],"date-time":"2019-08-12T06:38:02Z","timestamp":1565591882000},"page":"251","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":41,"title":["Antibiotic Resistance, Virulence Factors, Phenotyping, and Genotyping of E. coli Isolated from the Feces of Healthy Subjects"],"prefix":"10.3390","volume":"7","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0944-6677","authenticated-orcid":false,"given":"Stefano","family":"Raimondi","sequence":"first","affiliation":[{"name":"Department of Life Sciences, University of Modena and Reggio Emilia, via Campi 103, 41125, Modena, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lucia","family":"Righini","sequence":"additional","affiliation":[{"name":"Department of Life Sciences, University of Modena and Reggio Emilia, via Campi 103, 41125, Modena, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francesco","family":"Candeliere","sequence":"additional","affiliation":[{"name":"Department of Life Sciences, University of Modena and Reggio Emilia, via Campi 103, 41125, Modena, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eliana","family":"Musmeci","sequence":"additional","affiliation":[{"name":"Department of Life Sciences, University of Modena and Reggio Emilia, via Campi 103, 41125, Modena, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8101-9835","authenticated-orcid":false,"given":"Francesca","family":"Bonvicini","sequence":"additional","affiliation":[{"name":"Department of Pharmacy and Biotechnology, Alma Mater Studiorum-University of Bologna, Via Massarenti 9, 40138 Bologna, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giovanna","family":"Gentilomi","sequence":"additional","affiliation":[{"name":"Department of Pharmacy and Biotechnology, Alma Mater Studiorum-University of Bologna, Via Massarenti 9, 40138 Bologna, Italy"},{"name":"Unit of Microbiology, Alma Mater Studiorum-University of Bologna, S. Orsola-Malpighi Hospital, Via Massarenti 9, 40138 Bologna, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0200-573X","authenticated-orcid":false,"given":"Marjanca","family":"Star\u010di\u010d Erjavec","sequence":"additional","affiliation":[{"name":"Department of Biology, Biotechnical Faculty, University of Ljubljana, Jamnikarjeva 101, 1000 Ljubljana, Slovenia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alberto","family":"Amaretti","sequence":"additional","affiliation":[{"name":"Department of Life Sciences, University of Modena and Reggio Emilia, via Campi 103, 41125, Modena, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maddalena","family":"Rossi","sequence":"additional","affiliation":[{"name":"Department of Life Sciences, University of Modena and Reggio Emilia, via Campi 103, 41125, Modena, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,8,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1753","DOI":"10.1086\/315418","article-title":"A proposal for an inclusive designation for extraintestinal pathogenic Escherichia coli: ExPEC","volume":"181","author":"Russo","year":"2000","journal-title":"J. Infect. Dis."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Manges, A.R., Geum, H.M., Guo, A., Edens, T.J., Fibke, C.D., and Pitout, J.D.D. (2019). Global extraintestinal pathogenic Escherichia coli (ExPEC) lineages. Clin. Microbiol. Rev., 32.","DOI":"10.1128\/CMR.00135-18"},{"key":"ref_3","first-page":"3","article-title":"E. coli as an all-rounder: The thin line between commensalism and pathogenicity","volume":"358","author":"Leimbach","year":"2013","journal-title":"Curr. Top Microbiol. Immunol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1128\/CMR.00022-13","article-title":"Recent advances in understanding enteric pathogenic Escherichia coli","volume":"26","author":"Croxen","year":"2013","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1186\/s13099-019-0290-0","article-title":"Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: Recent reports","volume":"11","author":"Sarowska","year":"2019","journal-title":"Gut Pathog."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Searle, L.J., M\u00e9ric, G., Porcelli, I., Sheppard, S.K., and Lucchini, S. (2015). Variation in siderophore biosynthetic gene distribution and production across environmental and faecal populations of Escherichia coli. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0117906"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Welch, R.A. (2016). Uropathogenic Escherichia coli-Associated Exotoxins. Microbiol. Spectr., 4.","DOI":"10.1128\/microbiolspec.UTI-0011-2012"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Kaas, R.S., Friis, C., Ussery, D.W., and Aarestrup, F.M. (2012). Estimating variation within the genes and inferring the phylogeny of 186 sequenced diverse Escherichia coli genomes. BMC Genom., 13.","DOI":"10.1186\/1471-2164-13-577"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/ecosalplus.esp-0003-2018","article-title":"Spread and persistence of virulence and antibiotic resistance genes: A ride on the F plasmid conjugation module","volume":"8","author":"Koraimann","year":"2018","journal-title":"EcoSal Plus"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1086\/315217","article-title":"Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise","volume":"181","author":"Johnson","year":"2000","journal-title":"J. Infect. Dis."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Kudinha, T., Johnson, J.R., Andrew, S.D., Kong, F., Anderson, P., and Gilbert, G.L. (2013). Distribution of phylogenetic groups, sequence type ST131, and virulence-associated traits among Escherichia coli isolates from men with pyelonephritis or cystitis and healthy controls. Clin. Microbiol. Infect., 19.","DOI":"10.1111\/1469-0691.12123"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Lee, J.G., Han, D.S., Jo, S.V., Lee, A.R., Park, C.H., Eun, C.S., and Lee, Y. (2019). Characteristics and pathogenic role of adherent-invasive Escherichia coli in inflammatory bowel disease: Potential impact on clinical outcomes. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0216165"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1331","DOI":"10.1099\/jmm.0.022475-0","article-title":"Commensal Escherichia coli of healthy humans: A reservoir for antibiotic-resistance determinants","volume":"59","author":"Bailey","year":"2010","journal-title":"J. Med. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1089\/mdr.2014.0031","article-title":"Fecal carriage rates of extended-spectrum \u03b2-lactamase-producing Escherichia coli among antibiotic naive healthy human volunteers","volume":"21","author":"Mathai","year":"2015","journal-title":"Microb. Drug Resist."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Gonz\u00e1lez, D., Gallagher, E., Z\u00fa\u00f1iga, T., Leiva, J., and Vitas, A.I. (2019). Prevalence and characterization of \u03b2-lactamase-producing Enterobacteriaceae in healthy human carriers. Int. Microbio., in press.","DOI":"10.1007\/s10123-019-00087-z"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"4555","DOI":"10.1128\/AEM.66.10.4555-4558.2000","article-title":"Rapid and simple determination of the Escherichia coli phylogenetic group","volume":"66","author":"Clermont","year":"2000","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1111\/1758-2229.12019","article-title":"The Clermont Escherichia coli phylo-typing method revisited: Improvement of specificity and detection of new phylo-groups","volume":"5","author":"Clermont","year":"2013","journal-title":"Environ. Microbiol. Rep."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1080\/1040841X.2018.1481013","article-title":"E. coli and colorectal cancer: A complex relationship that deserves a critical mindset","volume":"44","author":"Wassenaar","year":"2018","journal-title":"Crit. Rev. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1128\/mr.58.2.162-210.1994","article-title":"Analysis of the sequence and gene products of the transfer region of the F sex factor","volume":"58","author":"Frost","year":"1994","journal-title":"Microbiol. Rev."},{"key":"ref_20","first-page":"91","article-title":"Cloning and characterization of the ColE7 plasmid","volume":"137","author":"Chak","year":"1991","journal-title":"J. Gen. Microbiol."},{"key":"ref_21","unstructured":"Raimondi, S., Amaretti, A., Gentilomi, G., Bonvicini, F., and Rossi, M. Antibiotic resistance, virulence factors, phenotyping, and genotyping of Enterobacteriaceae (other than E. coli) isolated from the feces of healthy subjects, Unpublished; manuscript in preparation."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1078","DOI":"10.1086\/427996","article-title":"Escherichia coli strains belonging to phylogenetic group B2 have superior capacity to persist in the intestinal microflora of infants","volume":"191","author":"Nowrouzian","year":"2005","journal-title":"J. Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2303","DOI":"10.1128\/AEM.02405-10","article-title":"Pathogenicity island markers, virulence determinants malX and usp, and the capacity of Escherichia coli to persist in infants\u2019 commensal microbiotas","volume":"77","author":"Ostblom","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_24","first-page":"141","article-title":"Are Escherichia coli pathotypes still relevant in the era of whole-genome sequencing?","volume":"6","author":"Holt","year":"2016","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"5792","DOI":"10.1038\/ncomms6792","article-title":"Prediction of antibiotic resistance by gene expression profiles","volume":"5","author":"Suzuki","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1222","DOI":"10.1128\/AAC.00765-10","article-title":"Antimicrobial resistance in more than 100,000 Escherichia coli isolates according to culture site and patient age, gender, and location","volume":"55","author":"Selva","year":"2011","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Cole, B.K., Ilikj, M., McCloskey, C.B., and Chavez-Bueno, S. (2019). Antibiotic resistance and molecular characterization of bacteremia Escherichia coli isolates from newborns in the United States. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0219352"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Morley, V.J., Woods, R.J., and Read, A.F. (2019). Bystander selection for antimicrobial resistance: Implications for patient health. Trends in Microbiol., in press.","DOI":"10.1016\/j.tim.2019.06.004"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Dyar, O.J., Hoa, N.Q., Trung, N.V., Phuc, H.D., Larsson, M., Chuc, N.T., and Lundborg, C.S. (2012). High prevalence of antibiotic resistance in commensal Escherichia coli among children in rural Vietnam. BMC Infect. Dis., 12.","DOI":"10.1186\/1471-2334-12-92"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1862","DOI":"10.1093\/infdis\/jiv278","article-title":"Gut colonization of healthy children and their mothers with pathogenic ciprofloxacin-resistant Escherichia coli","volume":"212","author":"Gurnee","year":"2015","journal-title":"J. Infect. Dis."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"546","DOI":"10.1007\/s00248-018-1228-7","article-title":"insights into antimicrobial resistance traits of commensal human gut microbiota","volume":"77","author":"Bag","year":"2019","journal-title":"Microb. Ecol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"6682","DOI":"10.1038\/s41598-019-43227-1","article-title":"High levels of drug resistance in commensal E. coli in a cohort of children from rural central India","volume":"9","author":"Purohit","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1111\/1462-2920.14009","article-title":"Antibiotic resistome in a large-scale healthy human gut microbiota deciphered by metagenomic and network analyses","volume":"20","author":"Feng","year":"2018","journal-title":"Environ. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1181","DOI":"10.2147\/IDR.S201324","article-title":"Prevalence of antibiotic resistance in Escherichia coli strains simultaneously isolated from humans, animals, food, and the environment: A systematic review and meta-analysis","volume":"12","author":"Pormohammad","year":"2019","journal-title":"Infect. Drug Resist."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"4115","DOI":"10.1128\/IAI.00752-12","article-title":"Escherichia coli isolates that carry vat, fyuA, chuA, and yfcV efficiently colonize the urinary tract","volume":"80","author":"Spurbeck","year":"2012","journal-title":"Infect. Immun."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1128\/CMR.18.2.264-292.2005","article-title":"Pathogenesis of Afa\/Dr. diffusely adhering Escherichia coli","volume":"18","author":"Servin","year":"2005","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Biesecker, S.G., Nicastro, L.K., Wilson, R.P., and T\u00fckel, \u00c7. (2018). The functional amyloid curli protects Escherichia coli against complement-mediated bactericidal activity. Biomolecules, 8.","DOI":"10.3390\/biom8010005"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.ijantimicag.2017.10.004","article-title":"Integrons in Enterobacteriaceae: Diversity, distribution and epidemiology","volume":"51","author":"Kaushik","year":"2018","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3906","DOI":"10.1128\/JCM.00949-08","article-title":"Molecular epidemiology and phylogenetic distribution of the Escherichia coli pks genomic island","volume":"46","author":"Johnson","year":"2008","journal-title":"J. Clin. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"856","DOI":"10.1093\/infdis\/jiv506","article-title":"HlyF produced by extraintestinal pathogenic Escherichia coli is a virulence factor that regulates outer membrane vesicle biogenesis","volume":"213","author":"Murase","year":"2016","journal-title":"J. Infect. Dis."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1099\/mic.0.25858-0","article-title":"A novel ColV plasmid encoding type IV pili","volume":"149","author":"Gophna","year":"2003","journal-title":"Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.plasmid.2015.10.001","article-title":"Strain \u017dP\u2014The first bacterial conjugation-based \u201ckill\u201d-\u201d anti-kill\u201d antimicrobial system","volume":"82","author":"Kuznetsova","year":"2015","journal-title":"Plasmid"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1111\/lam.12884","article-title":"Estimation of the bacteriocin ColE7 conjugation-based \u201ckill\u201d - \u201canti-kill\u201d antimicrobial system by real-time PCR, fluorescence staining and bioluminescence assays","volume":"67","author":"Maslennikova","year":"2018","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1156","DOI":"10.1093\/molbev\/msj125","article-title":"Enterobacterial repetitive intergenic consensus (ERIC) sequences in Escherichia coli: Evolution and implications for ERIC-PCR","volume":"23","author":"Wilson","year":"2006","journal-title":"Mol. Biol. Evol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.anaerobe.2015.10.006","article-title":"Comparison of culture-dependent and independent approaches to characterize fecal bifidobacteria and lactobacilli","volume":"38","author":"Quartieri","year":"2016","journal-title":"Anaerobe"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Simone, M., Gozzoli, C., Quartieri, A., Mazzola, G., Di Gioia, D., Amaretti, A., Raimondi, S., and Rossi, M. (2014). The probiotic Bifidobacterium breve B632 inhibited the growth of Enterobacteriaceae within colicky infant microbiota cultures. Biomed. Res. Int.","DOI":"10.1155\/2014\/301053"},{"key":"ref_47","unstructured":"(2019, July 19). Standard Operating Procedure for PulseNet PFGE of Escherichia coli O157:H7, Escherichia coli non-O157 (STEC), Salmonella serotypes, Shigella sonnei and Shigella flexneri, Available online: http:\/\/www.cdc.gov\/pulsenet\/PDF\/ecoli-shigella-salmonella-pfge-protocol-508c.pdf."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Johnson, J.R., Porter, S., Johnston, B., Kuskowski, M.A., Spurbeck, R.R., Mobley, H.L., and Williamson, D.A. (2015). Host characteristics and bacterial traits predict experimental virulence for Escherichia coli bloodstream isolates from patients with urosepsis. Open Forum Infect. Dis., 2.","DOI":"10.1093\/ofid\/ofv083"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.micpath.2017.10.009","article-title":"Genetic diversity, phylogroup distribution and virulence gene profile of pks positive Escherichia coli colonizing human intestinal polyps","volume":"112","author":"Sarshar","year":"2017","journal-title":"Microb. Pathog."},{"key":"ref_50","first-page":"10","article-title":"N-Acetyl-glucosamine influences the biofilm formation of Escherichia coli","volume":"22","author":"Sicard","year":"2018","journal-title":"Gut Pathog."},{"key":"ref_51","first-page":"1448","article-title":"Biofilm-forming abilities of shiga toxin-producing Escherichia coli isolates associated with human infections","volume":"28","author":"Vogeleer","year":"2015","journal-title":"Appl. Environ. Microbiol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/7\/8\/251\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:10:09Z","timestamp":1760188209000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/7\/8\/251"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,8,10]]},"references-count":51,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2019,8]]}},"alternative-id":["microorganisms7080251"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms7080251","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,8,10]]}}}